Clinical P r a c t i c e Rationale for Socket Preservation after Extraction of a Single-Rooted Tooth when Planning for Future Implant Placement

Contact Author Tassos Irinakis, DDS, Dip Perio, MSc, FRCD(C) Dr. Irinakis Email: irinakis@ interchange.ubc.ca ABSTRACT

After tooth extraction, the alveolar ridge will commonly decrease in volume and change morphologically. These changes are usually clinically significant and can make placement of a conventional bridge or an implant-supported crown difficult. If bone resorption is significant enough, then placement of an implant may become extremely challenging. Postextraction maintenance of the alveolar ridge minimizes residual ridge resorption and, thus, allows placement of an implant that satisfies esthetic and functional criteria. Recent advances in materials and techniques allow the dentist to place implants in sites that were considered compromised in the past. This article focuses on the healing pattern of sockets, with and without the use of regenerative materials, and the rationale for preserving the dimensions of the extraction socket. Histologic and clinical evidence is reviewed to provide an in-depth understanding of the logic behind and value of socket preservation.

© J Can Dent Assoc 2006; 72(10):917–22 MeSH Key Words: alveolar bone loss/prevention & control; bone regeneration; tooth extraction/ This article has been peer reviewed. adverse effects; wound healing

oss of alveolar bone may be attributed to fabrication of an implant-supported restora- a variety of factors, such as endodontic tion or a conventional prosthesis; and it may Lpathology, periodontitis, facial trauma make the placement of an implant challenging and aggressive maneuvers during extractions. if not unfeasible.3 However, it is possible to Millions of teeth are still extracted annually minimize such problems by simply carrying in North America. Most extractions are done out ridge preservation procedures in extrac- with no regard for maintaining the alveolar tion sockets using grafting materials with or ridge.1,2 without barrier membranes.4,5 Several studies, Whether due to caries, trauma or ad- clinical case series and literature reviews in vanced , tooth extrac- peer-reviewed journals were examined in de- tion and subsequent healing of the socket tail to establish a rationale for using socket commonly result in osseous deformities of preservation as a therapeutic option following the alveolar ridge, including reduced height tooth extraction. This review offers informa- (Fig. 1) and reduced width (Fig. 2) of the re- tion that can be useful to the clinician who sidual ridge.2 The severity of the healing pat- chooses to implement this procedure in his or tern may pose a problem for the clinician in her practice, but it should not be viewed as a 2 ways: it creates an esthetic problem in the “recipe” for socket preservation.

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connective tissue rich in vessels and inflammatory cells.10 By 4–6 weeks, most parts of the alveolus are filled with woven bone, while the soft tissue becomes keratinized. At 4–6 months, the mineral tissue within the ori- ginal socket is reinforced with layers of lamellar bone that is deposited on the previously formed woven bone.8–10 Although bone deposition in the socket will continue for sev- Figure 1: Reduced height of the alveolar Figure 2: “Collapse” of the buccal ridge following extraction of the lower left socket wall 2 months after extraction eral months, it will not reach the canine and first premolar. of the upper left central incisor. Bone coronal bone level of the neighbouring grafting will be necessary if the patient teeth.11 wants an implant. Patterns of Jaw Resorption Clinical and cephalometric studies from the 1950s to the 1970s described the resorption process in the postex- traction anterior ridge of the edentu- lous mandible.12–15 Atwood13 divided factors affecting the rate of resorption into 4 categories: anatomic, metabolic, functional and prosthetic. Tallgren16 demonstrated 400% higher residual Figure 3: The thin, fragile facial socket wall Figure 4: When a dehiscence is present, ridge resorption in the mandible com- of the upper anterior teeth is susceptible to the buccolingual dimension of the damage during extraction maneuvers. postextraction ridge is likely to pose pared with the maxilla. challenges for future implant placement. Regarding the surfaces most af- fected by extractions, some classic studies have demonstrated that postextraction alveolar resorption is Socket–Alveolus Healing significantly larger in the buccal aspect in both jaws.17–20 Jahangiri and others6 provide a current perspective on This can easily be understood if one looks closely at residual ridge remodelling, beginning with the cascade the labial anatomy of the alveolar bone surrounding the of inflammatory reactions that is activated immediately upper and lower teeth. The margins of the facial al- after tooth extraction. The socket fills with blood from veoli are thin, mostly cortical (though in rare cases, they the severed vessels, which contain proteins and damaged contain cancellous bone), knife-edged and frail (Fig. 3). When exposed to the trauma caused by extraction man- cells. These cells initiate a series of events that will lead euvers, the jaw bone is predisposed to resorptive patterns to the formation of a fibrin network, which, along with that may lead to unfavourable conditions for implant platelets, forms a “blood clot” or “coagulum” within the placement.2 Commonly, postextraction osseous remodel- first 24 hours.7 Acting as a physical matrix, the coagulum ling also takes place in the presence of dehiscences and directs the movement of cells, including mesenchymal fenestrations that magnify the problem, the end result cells, as well as growth factors. Neutrophils and later being buccal concavity in the alveolar bone (Fig. 4). macrophages enter the wound site and digest bacteria and The degree of residual ridge resorption is closely tissue debris to sterilize the wound. They release growth related to the time since tooth extraction14,21,22 — in factors and cytokines that will induce and amplify the both maxilla and mandible. The loss of tissue contour migration of mesenchymal cells and their synthetic ac- is greatest in the early postextraction period (within 8 tivity within the coagulum. 6 months).17–19 Apparently, the healing of sockets in the Within a few days, the blood clot begins to break maxilla progresses faster (because of the greater vascular down (fibrinolysis). The proliferation of mesenchymal supply) than those in the mandible, which could lead to a cells leads to gradual replacement of the coagulum by faster resorption pattern.23 granulation tissue (2–4 days).9 By the end of 1 week, a Several recent studies have examined resorption pat- vascular network is formed and by 2 weeks the marginal terns following single-tooth extraction. Using subtrac- portion of the extraction socket is covered with young tion radiography, Schropp and others11 assessed, in a

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Table 1 Advantages, disadvantages and examples of the 2 major membrane categories used in guided bone regeneration procedures including socket preservation

Membrane category Advantages Disadvantages Commercial examples Nonresorbable • Numerous studies demonstrate • Require a second surgery for • ePTFE membranes, e.g., their success removal Gore-Tex (Gore Medical, • May be titanium reinforced • Increase patient morbidity Flagstaff, Ariz.) • Remain intact until removal • If exposed, must be removed • Titanium-reinforced Gore-Tex • Easily attached with titanium or • Can be technique sensitive resorbable tacks • Greater bone fill if membrane not exposed • Minimal tissue response if membrane not exposed

Resorbable • Numerous studies demonstrate • Uncertain duration of • Neomem (bovine collagen their success function matrix; Citagenix Inc., • Does not require surgical removal • Difficult to tack down Laval, Que.) • Decreased patient morbidity • Slightly less bone fill than • Bio-Gide (porcine collagen • Improved soft-tissue healing nonresorbable membranes matrix; Geistlich AG, Wolhusen, • Tissue-friendly reaction to • Inflammatory response Switzerland) membrane exposure from tissues may interfere • Ossix (cross-linked collagen • Cost effective; one surgery only with healing and GBR barrier; Implant Innovations Inc., • Does not have to be removed if • Can be technique sensitive Palm Beach Gardens, Fla.) exposed ePTFE = expanded polytetrafluoroethylene; GBR = guided bone regeneration

12-month prospective study, bone formation in the al- 1.32 mm, respectively, considerably less than the average veolus and changes in the contour of the alveolar pro- loss in sockets that healed naturally. In addition, the cess following single-tooth extraction. The width of the quality of the bone in sockets that have healed in the alveolar ridge decreased 50% (from 12 mm to 5.9 mm, presence of a barrier membrane is excellent for implant on average), and two-thirds of the reduction occurred placement.24 within the first 3 months. The percentage reduction was A wide range of barrier membranes have been used somewhat larger in the molar compared with the pre- in numerous studies over the years, e.g., expanded poly- molar region. Changes in bone height, however, were tetrafluoroethylene (ePTFE), collagen, polyglycolic acid only slight (less than 1 mm). The level of bone regener- and polyglactin 910. However, these can be grouped into ated in the extraction socket never reached the coronal 2 major categories: nonresorbable and resorbable mem- level of bone attached to the tooth surfaces distal and branes. The advantages and disadvantages of various mesial to the extraction site. The bone surface becomes membranes are presented in Table 1 along with examples “curved” apically. of commercial products. As the time for resorption of Lekovic and coworkers3 evaluated the clinical ef- these membranes differs, the clinician should follow fectiveness of a bioabsorbable membrane in preserving manufacturers’ directions. alveolar ridges following single-tooth extraction in a The literature justifies the use of bone grafting ma- split-mouth prospective study. At the 6-month re-entry terials in freshly extracted sockets.25,26 When demineral- appointment, they found an average loss of alveolar ized freeze-dried bone allograft (DFDBA) was used in height and width of 1.50 mm and 4.56 mm, respectively, conjunction with a collagen membrane, the width of the in the healed sockets. alveolar ridge decreased from 9.2 mm to 8.0 mm, while the width of the socket sites that healed naturally de- Using Membranes and Bone Grafts in Sockets creased from 9.1 mm to 6.4 mm on average.25 In addition, In the study by Lekovic,3 the average loss of alveolar the average loss of bone height in the latter group was height and width in sockets that were left to heal with 1 mm, while the grafted sites actually gained height. Even only a membrane covering them was 0.38 mm and with no barrier membrane, a socket fill of nearly 85%

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Table 2 Sources of grafting material for guided bone regeneration Type of bone graft Source of the grafting material

Autogenous grafts Material is transferred from one position to another within the same individual. Graft may be (autografts) intraoral or extraoral depending on the site of harvest. Allografts Material is transferred from a donor of the same species. The most common grafts are freeze-dried bone grafts, which may be mineralized or demineralized. Xenografts Material is transferred from a donor of another species, processed appropriately. Primarily porous deproteinized bovine bone mineral. Alloplasts Synthetic materials, usually inert, used as a substitute for bone grafts.

can be achieved by placing porous bovine bone mineral Valentini and colleagues33 found that BIC at sites grafted in fresh extraction sites.26 with bovine bone mineral was greater than or equal to that in nongrafted sites; histologic analysis 6 months Bone-to-Implant Contact in Grafted Sockets after grafting showed a BIC of 73% in grafted vs. 63% in Some researchers might argue that the quality of the nongrafted areas. Comparison of the torque necessary bone in grafted sockets may not be adequate for im- to remove implants 6 months after placement showed no plant placement. Thus, various grafting materials have statistically significant differences between grafted and been used to preserve the socket or augment the lateral nongrafted sites, supporting the successful osseointegra- ridge before implant placement (Table 2). When pla- tion of implants in grafted sites.34 cing xenografts (Fig. 5) or DFDBA in fresh extraction Success rates are also satisfactory when placing im- sockets, Becker and others27 found that there was min- plants in previously grafted bone. In a restrospective imal vital bone-to-implant contact (BIC). However, in study of 607 titanium plasma sprayed implants placed this study, the histologic core samples were taken within in regenerated bone (with DFDBA), 97.2% of maxilla 3–6 months of extraction when it is common to wait implants and 97.4% of mandible implants were successful 6–9 months to place implants when using these materials. for an average of 11 years.35 Even higher success rates Thus, the cores may have been taken too early to provide in augmented bone have been reported by Simion and appropriate information. In a different study examining coworkers.36 These numbers compare very favourably the healing of sockets filled with bioactive glass (allo- with the success rates for implants placed in pristine plastic synthetic bone substitute), a very long healing bone.37–41 time was required for even a small amount of new bone to be incorporated into the graft.28 Conclusions Several studies have investigated BIC between regener- The success of osseointegrated dental implants de- ated or natural bone and rough or machined-surface pends on whether there is a sufficient volume of healthy implants. Trisi and colleagues29 examined the posterior bone at the recipient site at the time of implant place- maxilla, where bone is generally of poor quality, investi- ment. The placement of an implant at a site with a thin gating the BIC at 2 and 6 months. For rough-surfaced im- crestal ridge (e.g., postextraction ridge) could result in plants (dual acid-etched), there was 48% BIC at 2 months a significant buccal dehiscence. Thus, it seems prudent and 72% BIC at 6 months, compared with only 19% to prevent alveolar ridge destruction and make efforts to and 34%, respectively, for machined-surface implants. preserve it during extraction procedures. Similar results were noted in an animal study, in which Maintenance of an extraction socket for future implant there was 74% BIC in type IV bone (poor-quality bone) therapy does not exclude immediate implant placement, at 6 months on titanium porous oxide (TiUnite, Nobel but knowledge and experience are needed to determine Biocare, Gothenburg, Sweden) implants.30 the best treatment modality. Postextraction treatment When sockets are filled with grafting material, graft options may include, but are not limited to, immediate remnants usually remain at the time of implant place- implant placement; natural socket healing and delayed ment. In one study,31 bovine bone mineral contained implant placement; natural healing and future osseous about 30% particles at 6 months. In a different study32 ridge augmentation (for implant or fixed partial denture); in which DFDBA was used, the rate at which graft ma- natural healing and future soft tissue ridge augmentation terial was replaced by new vital bone was very slow and (for fixed partial denture); natural healing and removable incomplete even at 4 years; however, from a clinical point partial denture. of view, the load-bearing capacity of the regenerated There are various reasons why the surgeon may not bone appeared to be similar to that of normal bone. wish to follow a particular treatment option. These

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a b c

d e f

Figure 5: Upper lateral incisor (a) that was extracted using periotomes (thus avoiding trauma to the socket walls); its socket (b) was then filled with porous bovine bone mineral c( ). Images d to f were taken after 6 months of healing and show successful preservation of the ridge for placement of a narrow-platform implant.

reasons could also be viewed as limitations to socket THE AUTHOR preservation with bone grafting. Examples of potential problems are lack of adequate apical bone to begin with Dr. Irinakis is associate clinical professor and director of for primary anchorage of the implant; lack of buccal graduate periodontics and implant surgery at the University of British Columbia, Vancouver, British Columbia. He is also socket wall; area where esthetics are important and the in part-time private practice in periodontics and implant surgeon prefers to wait for tissue settlement; the indi- in Vancouver and Coquitlam, B.C. cations for immediate implant placement are stronger; Correspondence to: Dr. Tassos Irinakis, Faculty of Dentistry, University lack of experience of the dentist in selecting appropriate of British Columbia, 2199 Wesbrook Mall, Vancouver, BC V6T 1Z3. materials and techniques; indecisive patient; inability of The author has no declared financial interests in any company manufac- patient to cover the cost. turing the types of products mentioned in this article. Regardless of the reasons for socket preservation, there seems to be a consensus that sufficient alveolar References 1. Marcus SE, Drury TF, Brown LJ, Zion GR. Tooth retention and tooth loss bone volume and favourable architecture of the alveolar in the permanent dentition of adults: United States, 1988–1991. J Dent Res ridge are essential to achieve ideal functional and esthetic 1996; 75(Spec no.):684–95. prosthetic reconstruction following implant therapy.1 2. Mecall RA, Rosenfeld AL. Influence of residual ridge resorption pat- terns on implant fixture placement and tooth position. 1. Int J Periodontics Preserving or reconstructing the extraction socket of a Restorative Dent 1991; 11(1):8–23. failed tooth according to the principles of guided bone 3. Lekovic V, Camargo PM, Klokkevold PR, Weinlaender M, Kenney EB, Dimitrijevic B, and other. Preservation of alveolar bone in extraction sockets regeneration enhances our ability to provide esthetically using bioabsorbable membranes. J Periodontol 1998; 69(9):1044–9. pleasing restorations to our patients without violating the 4. Zubillaga G, Von Hagen S, Simon BI, Deasy MJ. Changes in alveolar bone predictability and function of those prostheses. a height and width following post-extraction ridge augmentation using a

���JCDA • www.cda-adc.ca/jcda • December 2006/January 2007, Vol. 72, No. 10 • 921 ––– Irinakis ––– Clinical P r a c t i c e fixed bioabsorbable membrane and demineralized freeze-dried bone osteo- 32. Simion M, Trisi P, Piattelli A. GBR with an e-PTFE membrane associ- inductive graft. J Periodontol 2003; 74(7):965–75. ated with DFDBA: histologic and histochemical analysis in a human implant 5. Winkler S. Implant site development and alveolar bone resorption pat- retrieved after 4 years of loading. Int J Periodontics Restorative Dent 1996; terns. J Oral Implantol 2002; 28(5):226–9. 16(4):338–47. 6. Jahangiri L, Devlin H, Ting K, Nishimura I. Current perspectives in residual 33. Valentini P, Abensur D, Densari D, Graziani JN, Hammerle C. Histological ridge remodeling and its clinical implications: a review. J Prosthet Dent 1998; evaluation of Bio-Oss in a 2-stage sinus floor elevation and implantation pro- 80(2):224–37. cedure. A human case report. Clin Oral Implants Res 1998; 9(1):59–64. 7. Amler MH. The time sequence of tissue regeneration in human extraction 34. Kohal RJ, Mellas P, Hurzeler MB, Trejo PM, Morrison E, Caffesse RG. The wounds. Oral Surg Oral Med Oral Pathol 1969; 27(3):309–18. effects of guided bone regeneration and grafting on implants placed into immediate extraction sockets. An experimental study in dogs. J Periodontol 8. Lin WL, McCulloch CA, Cho MI. Differentiation of periodontal ligament 1998; 69(8):927–37. fibroblasts into osteoblasts during socket healing after tooth extraction in the rat. Anat Rec 1994; 240(4):492–506. 35. Fugazzotto PA. Success and failure rates of osseointegrated implants in function in regenerated bone for 72 to 133 months. Int J Oral Maxillofac 9. Araujo MG, Berglundh T, Lindhe J. On the dynamics of periodontal tissue Implants 2005; 20(1):77–83. formation in degree III furcation defects. An experimental study in dogs. J Clin Periodontol 1997; 24(10):738–46. 36. Simion M, Jovanovic SA, Tinti C, Benfenati SP. Long-term evaluation of osseointegrated implants inserted at the time or after vertical ridge aug- 10. Cardaropoli G, Araujo M, Lindhe J. Dynamics of bone tissue formation mentation. A retrospective study on 123 implants with 1–5 year follow-up. in tooth extraction sites. An experimental study in dogs. J Clin Periodontol Clin Oral Implants Res 2001; 12(1):35–45. 2003; 30(9):809–18. 37. Karoussis IK, Bragger U, Salvi GE, Burgin W, Lang NP. �������������Effect of im- 11. Schropp L, Wenzel A, Kostopoulos L, Karring T. Bone healing and soft plant design on survival and success rates of titanium oral implants: a 10- tissue contour changes following single-tooth extraction: a clinical and year prospective cohort study of the ITI System. Clin Oral radiographic 12-month prospective study. Int J Periodontics Restorative Dent Implants Res 2004; 15(1):8–17. 2003; 23(4):313–23. 38. Buser D, Mericske-Stern R, Bernard JP, Behneke A, Behneke N, Hirt HP, 12. Atwood DA. Some clinical factors related to rate of resorption of residual and others. �����������������������������������������������������������Long-term evaluation of non-submerged ITI implants. Part 1: ridges. �����1962. J Prosthet Dent 2001; 86(2):119–25. 8-year life table analysis of a prospective multi-center study with 2359 im- 13. Atwood DA. A cephalometric study of the clinical rest position of the plants. Clin Oral Implants Res 1997; 8(3):161–72. mandible. Part II. The variability in the rate of bone loss following the re- 39. Romeo E, Chiapasco M, Ghisolfi M, Vogel G. Long-term clinical effective- moval of occlusal contacts. J Prosthet Dent 1957; 7:544–52. ness of oral implants in the treatment of partial edentulism. Seven-year life 14. Tallgren A. The continuing reduction of the residual alveolar ridges in table analysis of a prospective study with ITI dental implants system used for complete denture wearers: a mixed-longitudinal study covering 25 years. single-tooth restorations. Clin Oral Implants Res 2002; 13(2):133–43. J Prosthet Dent 1972; 27(2):120–32. 40. Ferrigno N, Laureti M, Fanali S, Grippaudo G. A long-term follow-up 15. Carlsson GE, Bergman B, Hedegard B. Changes in contour of the maxil- study of non-submerged ITI implants in the treatment of totally edentulous lary under immediate . A longitudinal clinical and jaws. Part I: Ten-year life table analysis of a prospective multicenter study x-ray cephalometric study covering 5 years. Acta Odontol Scand 1967; with 1286 implants. Clin Oral Implants Res 2002;13(3):260–73. 25(1):45–75. 41. Fugazzotto PA, Beagle JR, Ganeles J, Jaffin R, Vlassis J, Kumar A. Success 16. Tallgren A. Changes in adult face height due to aging, wear and loss of and failure rates of 9 mm or shorter implants in the replacement of missing teeth and prosthetic treatment. Acta Odontol Scand 1957; 15(suppl. 24); maxillary molars when restored with individual crowns: preliminary results 73–122. 0 to 84 months in function. A retrospective study. J Periodontol 2004; 17. Pietrokovski J, Massler M. Alveolar ridge resorption following tooth ex- 75(2):327–32. traction. J Prosthet Dent 1967; 17(1):21–7. 18. Johnson K. A study of the dimensional changes occurring in the maxilla following tooth extraction. Aust Dent J 1969; 14(4):241–4. 19. Lam RV. Contour changes of the alveolar processes following extrac- tions. J Prosthet Dent 1960; 10:25–32. 20. Carlsson GE, Persson G. Morphological changes of the mandible after extraction and wearing of dentures. A longitudinal, clinical, and x-ray ceph- alometric study covering 5 years. Odontol Revy 1967; 18(1):27–54. 21. Humphries S, Devlin H, Worthington H. A radiographic investigation into bone resorption of mandibular alveolar bone in elderly edentulous adults. J Dent 1989; 17(2):94–6. 22. Ulm C, Solar P, Blahout R, Matejka M, Gruber H. Reduction of the com- pact and cancellous bone substances of the edentulous mandible caused by resorption. Oral Surg Oral Med Oral Pathol 1992; 74(2):131–6. 23. Soehren SE, Van Swol RL. The��������������������������������������������� healing extraction site: a donor area for periodontal grafting material. J Periodontol 1979; 50(3):128–33. 24. Carmagnola D, Adriaens P, Berglundh T. Healing of human extraction sockets filled with Bio-Oss. Clin Oral Implants Res 2003; 14(2):137–43. 25. Iasella JM, Greenwell H, Miller RL, Hill M, Drisko C, Bohra AA, and other. Ridge preservation with freeze-dried bone allograft and a collagen mem- brane compared to extraction alone for implant site development: a clinical and histologic study in humans. J Periodontol 2003; 74(7):990–9. 26. Artzi Z, Tal H, Dayan D. Porous bovine bone mineral in healing of human extraction sockets. Part 1: Histomorphometric evaluations at 9 months. J Periodontol 2000; 71(6):1015–23. 27. Becker W, Clokie C, Sennerby L, Urist MR, Becker BE. Histologic find- ings after implantation and evaluation of different grafting materials and titanium micro screws into extraction sockets: case reports. J Periodontol 1998; 69(4):414–21. 28. Norton MR, Wilson J. Dental implants placed in extraction sites im- planted with bioactive glass: human histology and clinical outcome. Int J Oral Maxillofac Implants 2002; 17(2):249–57. 29. Trisi P, Lazzara R, Rebaudi A, Rao W, Testori T, Porter SS. ������������Bone-implant contact on machined and dual acid-etched surfaces after 2 months of healing in the human maxilla. J Periodontol 2003; 74(7):945–56. 30. Huang YH, Xiropaidis A, Sorensen RG, Albandar JM, Hall J, Wikesjo UM. Bone formation at titanium porous oxide (TiUnite) oral implants in type IV bone. Clin Oral Implants Res 2005; 16(1):105–11. 31. Zitzmann NU, Scharer P, Marinello CP, Schupbach P, Berglundh T. Alveolar ridge augmentation with Bio-Oss: a histologic study in humans. Int J Periodontics Restorative Dent 2001; 21(3):288–95.

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